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Symbiotic Origin of Eukaryotic Nucleus: From Cell Body to Neo-Energide

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Concepts in Cell Biology - History and Evolution

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 23))

Abstract

Several aspects of the eukaryotic cell suggest that the nucleus is of symbiotic origin. The nucleus forms, via its perinuclear structures, the primary eukaryotic agent known also as the “cell body” or “energide.” New energides are generated only from other energides, as is the case for all other endosymbiotic organelles. Moreover, the energide can use its secretory apparatus to generate de novo the cell periphery apparatus. In contrast, the energide cannot be generated de novo. All this suggests that the energide was the primary symbiont of the eukaryotic cell and enslaved the host cell by stripping it of its DNA. The energide took control over the host cell that provided it with a protective niche. This feature, supported by other relevant data, suggests that the endoplasmic reticulum (ER) is a secondary organelle generated by the outer portion of the nuclear membrane. The ER represents a specialized domain of the outer nuclear envelope, which orchestrates the energide’s secretory and lytic activities via the ER network, Golgi apparatus, autophagy network, and lysosomes. In this way, the energide integrates the eukaryotic cell via ER/organelle/plasma membrane contact sites into a coherent agent of eukaryotic life. In addition, the plasma membrane provides feedback to the energide and renders protection via the plasma membrane-derived endosomal network. Recent new discoveries suggest archaeal origins for both the energide and its host cell.

Motto: Omnis Energide e Energide

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References

  • Abodeely M, DuBois KN, Hehl A, Stefanic S, Sajid M, DeSouza W, Attias M, Engel JC, Hsieh I, Fetter RD, McKerrow JH (2009) A contiguous compartment functions as endoplasmic reticulum and endosome/lysosome in Giardia lamblia. Eukaryot Cell 8:1665–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ai E, Skop AR (2009) Endosomal recycling regulation during cytokinesis. Commun Integr Biol 2:444–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akendengue L, Trépout S, Graña M, Voegele A, Janke C, Raynal B, Chenal A, Marco S, Wehenkel AM (2017) Bacterial kinesin light chain (Bklc) links the Btub cytoskeleton to membranes. Sci Rep 7:45668

    Article  PubMed  PubMed Central  Google Scholar 

  • Ammar R, Torti D, Tsui K, Gebbia M, Durbic T, Bader GD, Giaever G, Nislow C (2012) Chromatin is an ancient innovation conserved between Archaea and Eukarya. ELife 1:e00078

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Apel ED, Lewis RM, Grady RM, Sanes JR (2000) Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J Biol Chem 275:31986–31995

    Article  CAS  PubMed  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88

    Article  CAS  PubMed  Google Scholar 

  • Archibald JM, Lane CE (2009) Going, going, not quite gone: nucleomorphs as a case study in nuclear genome reduction. J Hered 100:582–590

    Article  CAS  PubMed  Google Scholar 

  • Azimzadeh J (2014) Exploring the evolutionary history of centrosomes. Philos Trans R Soc B 369:20130453

    Article  CAS  Google Scholar 

  • Bailey KA, Marc F, Sandman K, Reeve JN (2002) Both DNA and histone fold sequences contribute to archaeal nucleosome stability. J Biol Chem 277:9293–9301

    Article  CAS  PubMed  Google Scholar 

  • Baluška F, Barlow PW (1993) The role of the microtubular cytoskeleton in determining nuclear chromatin structure and passage of maize root cells through the cell cycle. Eur J Cell Biol 61:160–167

    PubMed  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (1997) Nuclear components with microtubule organizing properties in multicellular eukaryotes: functional and evolutionary considerations. Int Rev Cytol 175:91–135

    Article  PubMed  Google Scholar 

  • Baluška F, Lichtscheidl IK, Volkmann D, Barlow PW (1998) The plant cell body: a cytoskeletal tool for cellular development and morphogenesis. Protoplasma 202:1–10

    Article  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2001) Motile plant cell body: a ‘bug’ within a ‘cage’. Trends Plant Sci 6:104–111

    Article  PubMed  Google Scholar 

  • Baluška F, Hlavacka A, Samaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 130:422–431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2004a) Eukaryotic cells and their cell bodies: cell theory revisited. Ann Bot 94:9–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2004b) Cell bodies in cage. Nature 428:371

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Liners F, Hlavacka A, Schlicht M, Van Cutsem P, McCurdy DW, Menzel D (2005) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Menzel D, Barlow PW (2006a) Cytokinesis in plant and animal cells: endosomes ‘shut the door’. Dev Biol 294:1–10

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2006b) Cell-cell channels and their implications for cell theory. In: Baluška F, Volkmann D, Barlow PW (eds) Cell-cell channels. Landes Bioscience, Austin & Springer, New York, pp 1–18

    Google Scholar 

  • Baluška F, Volkmann D, Menzel D, Barlow PW (2012) Strasburger’s legacy to mitosis and cytokinesis and its relevance for the cell theory. Protoplasma 249:1151–1162

    Article  PubMed  Google Scholar 

  • Bapaume L, Reinhardt D (2012) How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza. Front Plant Sci 3:223

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbieri E, Di Fiore PP, Sigismund S (2016) Endocytic control of signaling at the plasma membrane. Curr Opin Cell Biol 39:21–27

    Article  CAS  PubMed  Google Scholar 

  • Baum DA (2015) A comparison of autogenous theories for the origin of eukaryotic cells. Am J Bot 102:1954–1965

    Article  CAS  PubMed  Google Scholar 

  • Benchimol M (2005) The nuclei of Giardia lamblia – new ultrastructural observations. Arch Microbiol 183:160–168

    Article  CAS  PubMed  Google Scholar 

  • Benchimol M (2007) Giardia lamblia under microscopy – how this primitive protist divide. Funct Dev Embryol 1:57–69

    Google Scholar 

  • Bengtson S, Sallstedt T, Belivanova V, Whitehouse M (2017) Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biol 15:e2000735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bernander R, Lind AE, Ettema TJ (2011) An archaeal origin for the actin cytoskeleton: implications for eukaryogenesis. Commun Integr Biol 4:664–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhutta MS, McInerny CJ, Gould GW (2014) ESCRT function in cytokinesis: location, dynamics and regulation by mitotic kinases. Int J Mol Sci 15:21723–21739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Binarová P, Cenklová V, Hause B, Kubátová E, Lysák M, Dolezel J, Bögre L, Dráber P (2000) Nuclear gamma-tubulin during acentriolar plant mitosis. Plant Cell 12:433–442

    PubMed  PubMed Central  Google Scholar 

  • Blackman LM, Harper JD, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 78:297–304

    Article  CAS  PubMed  Google Scholar 

  • Bloemendal S, Kück U (2013) Cell-to-cell communication in plants, animals, and fungi: a comparative review. Naturwissenschaften 100:3–19

    Article  CAS  PubMed  Google Scholar 

  • Bonifacino JS, Lippincott-Schwartz J (2003) Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol 4:409–414

    Article  CAS  PubMed  Google Scholar 

  • Bornens M, Azimzadeh J (2007) Origin and evolution of the centrosome. Adv Exp Med Biol 607:119–129

    Article  PubMed  Google Scholar 

  • Bothe H, Melkonian M (2016) Obituary: Eberhard Schnepf (April 4, 1931–April 10, 2016). Protist 167:460–463

    Article  PubMed  Google Scholar 

  • Burkhardt P (2015) The origin and evolution of synaptic proteins – choanoflagellates lead the way. J Exp Biol 218:506–514

    Article  PubMed  Google Scholar 

  • Burkhardt P, Grønborg M, McDonald K, Sulur T, Wang Q, King N (2014) Evolutionary insights into premetazoan functions of the neuronal protein homer. Mol Biol Evol 31:2342–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6:a016147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burns JA, Zhang H, Hill E, Kim E, Kerney R (2017) Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis. ELife 6:e22054

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith T (1987) The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci 503:17–54

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1988) Origin of the cell nucleus. Bioessays 9:72–78

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int J Syst Evol Microbiol 52:297–354

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (2010) Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct 5:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chapman MJ, Dolan MF, Margulis L (2000) Centrioles and kinetosomes: form, function, and evolution. Q Rev Biol 75:409–429

    Article  CAS  PubMed  Google Scholar 

  • Chen JV, Buchwalter RA, Kao LR, Megraw TL (2017) A splice variant of centrosomin converts mitochondria to microtubule-organizing centers. Curr Biol 27:1928–1940

    Article  CAS  PubMed  Google Scholar 

  • Davidov Y, Jurkevitch E (2009) Predation between prokaryotes and the origin of eukaryotes. Bioessays 31:748–757

    Article  CAS  PubMed  Google Scholar 

  • Dawson SC (2010) An insider’s guide to the microtubule cytoskeleton of Giardia. Cell Microbiol 12:588–598

    Article  CAS  PubMed  Google Scholar 

  • Dawson SC, House SA (2010) Life with eight flagella: flagellar assembly and division in Giardia. Curr Opin Microbiol 13:480–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8:395–403

    Article  PubMed  CAS  Google Scholar 

  • de Nooijer S, Holland BR, Penny D (2009) The emergence of predators in early life: there was no Garden of Eden. PLoS One 4:e5507

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352:353–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng X, Fink G, Bharat TAM, He S, Kureisaite-Ciziene D, Löwe J (2017) Four-stranded mini microtubules formed by Prosthecobacter BtubAB show dynamic instability. Proc Natl Acad Sci U S A 114:E5950–E5958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dergai M, Iershov A, Novokhatska O, Pankivskyi S, Rynditch A (2016) Evolutionary changes on the way to clathrin-mediated endocytosis in animals. Genome Biol Evol 8:588–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2:e380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Devos DP, Gräf R, Field MC (2014) Evolution of nucleus. Curr Opin Cell Biol 28:8–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhonukshe P, Baluška F, Schlicht M, Hlavaćka A, Šamaj J, Friml J, Gadella TW Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150

    Article  CAS  PubMed  Google Scholar 

  • Dhonukshe P, Šamaj J, Baluška F, Friml J (2007) A unifying new model of cytokinesis for the dividing plant and animal cells. Bioessays 29:371–381

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Celis C, Risca VI, Hurtado F, Polka JK, Hansen SD, Maturana D, Lagos R, Mullins RD, Monasterio O (2017) Bacterial tubulin A/B exhibit polarized growth, mixed-polarity bundling, and destabilization by GTP hydrolysis. J Bacteriol 199. https://doi.org/10.1128/JB.00211-17

  • Dishinger JF, Kee HL, Jenkins PM, Fan S, Hurd TW, Hammond JW, Truong YN, Margolis B, Martens JR, Verhey KJ (2010) Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nat Cell Biol 12:703–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobson JR, Hong D, Barutcu AR, Wu H, Imbalzano AN, Lian JB, Stein JL, van Wijnen AJ, Nickerson JA, Stein GS (2017) Identifying nuclear matrix-attached DNA across the genome. J Cell Physiol 232:1295–1305

    Article  CAS  PubMed  Google Scholar 

  • Dolan MF, Melnitsky H, Margulis L, Kolnicki R (2002) Motility proteins and the origin of the nucleus. Anat Rec 268:290–301

    Article  CAS  PubMed  Google Scholar 

  • Doležal P, Smíd O, Rada P, Zubácová Z, Bursać D, Suták R, Nebesárová J, Lithgow T, Tachezy J (2005) Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci U S A 102:10924–10929

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Douglas EA (2014) Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harb Perspect Biol 6:a016113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT, Wu X, Reith M, Cavalier-Smith T, Maier UG (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096

    Article  CAS  PubMed  Google Scholar 

  • Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J (2011) Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A 108:4846–4851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elias EV, Quiroga R, Gottig N, Nakanishi H, Nash TE, Neiman A, Lujan HD (2008) Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J Biol Chem 283:35996–36010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espigat-Georger A, Dyachuk V, Chemin C, Emorine L, Merdes A (2016) Nuclear alignment in myotubes requires centrosome proteins recruited by nesprin-1. J Cell Sci 129:4227–4237

    Article  CAS  PubMed  Google Scholar 

  • Estrada-Navarrete G, Cruz-Mireles N, Lascano R, Alvarado-Affantranger X, Hernàndez A, Barraza A, Olivares JE, Arthikala MK, Cardenas L, Quinto C, Sanchez F (2016) An autophagy-related kinase is essential for the symbiotic relationship between Phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi. Plant Cell 28:2326–2341

    Article  CAS  PubMed Central  Google Scholar 

  • Ettema TJ, Bernander R (2009) Cell division and the ESCRT complex: a surprise from the archaea. Commun Integr Biol 2:86–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fant X, Srsen V, Espigat-Georger A, Merdes A (2009) Nuclei of non-muscle cells bind centrosome proteins upon fusion with differentiating myoblasts. PLoS One 4:e8303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Faso C, Hehl AB (2011) Membrane trafficking and organelle biogenesis in Giardia lamblia: use it or lose it. Int J Parasitol 41:471–480

    Article  CAS  PubMed  Google Scholar 

  • Field MC, Sali A, Rout MP (2011) On a bender – BARs, ESCRTs, COPs, and finally getting your coat. J Cell Biol 193:963–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Field MC, Koreny L, Rout MP (2014) Enriching the pore: splendid complexity from humble origins. Traffic 15:141–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemming W (1882) Zellsubstanz, Kern und Zelltheilung. Vogel, Leipzig

    Google Scholar 

  • Folker ES, Baylies MK (2013) Nuclear positioning in muscle development and disease. Front Physiol 4:363

    Article  PubMed  PubMed Central  Google Scholar 

  • Gentil J, Hempel F, Moog D, Zauner S, Maier UG (2017) Review: origin of complex algae by secondary endosymbiosis: a journey through time. Protoplasma. doi:https://doi.org/10.1007/s00709-017-1098-8

  • Gerace L, Michael D, Huber MD (2012) Nuclear lamina at the crossroads of the cytoplasm and nucleus. J Struct Biol 177:24–31

    Article  CAS  PubMed  Google Scholar 

  • Gesson K, Rescheneder P, Skoruppa MP, von Haeseler A, Dechat T, Foisner R (2016) A-type lamins bind both hetero- and euchromatin, the latter being regulated by lamina-associated polypeptide 2 alpha. Genome Res 26:462–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341

    Article  PubMed  Google Scholar 

  • Goldman JG (2012) Ad memoriam – Lynn Margulis (5.03.1938–22.11.2011). Stud Hist Biol 4:119–124

    Google Scholar 

  • González-Sánchez JC, Costa R, Devos DPO (2015) A multi-functional tubulovesicular network as the ancestral eukaryotic endomembrane system. Biology (Basel) 4:264–281

    Google Scholar 

  • Gould SB, Maier UG, Martin WF (2015) Protein import and the origin of red complex plastids. Curr Biol 25:R515–R521

    Article  CAS  PubMed  Google Scholar 

  • Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M (2005) Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc Natl Acad Sci U S A 102:4359–4364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gräf R, Batsios P, Meyer I (2015) Evolution of centrosomes and the nuclear lamina: Amoebozoan assets. Eur J Cell Biol 94:249–256

    Article  PubMed  CAS  Google Scholar 

  • Grau-Bové X, Sebé-Pedrós A, Ruiz-Trillo I (2015) The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Mol Biol Evol 32:726–739

    Article  PubMed  CAS  Google Scholar 

  • Gray MW (2017) Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol Biol Cell 28:1285–1287

    Article  PubMed  PubMed Central  Google Scholar 

  • Grosche C, Hempel F, Bolte K, Zauner S, Maier UG (2014) The periplastidal compartment: a naturally minimized eukaryotic cytoplasm. Curr Opin Microbiol 22:88–93

    Article  PubMed  Google Scholar 

  • Gu M, La Joie D, Chen OS, von Appen A, Ladinsky MS, Redd MJ, Nikolova L, Bjorkman PJ, Sundquist WI, Ullman KS, Frost A (2017) LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells. Proc Natl Acad Sci U S A 114:E2166–E2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gulluni F, Martini M, Hirsch E (2017) Cytokinetic abscission: phosphoinositides and ESCRTs direct the final cut. J Cell Biochem 118:3561–3568

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS, Golding GB (1996) The origin of the eukaryotic cell. Trends Biochem Sci 21:166–171

    Article  CAS  PubMed  Google Scholar 

  • Guy L, Ettema TJ (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol 19:580–587

    Article  CAS  PubMed  Google Scholar 

  • Guy L, Saw JH, Ettema TJ (2014) The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harb Perspect Biol 6:a016022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534

    Article  CAS  PubMed  Google Scholar 

  • Hardin WR, Li R, Xu J, Shelton AM, Alas GCM, Minin VN, Paredez AR (2017) Myosin-independent cytokinesis in Giardia utilizes flagella to coordinate force generation and direct membrane trafficking. Proc Natl Acad Sci U S A 114:E5854–E5863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harr JC, Luperchio TR, Wong X, Cohen E, Wheelan SJ, Reddy KL (2015) Directed targeting of chromatin to the nuclear lamina is mediated by chromatin state and A-type lamins. J Cell Biol 208:33–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartman H (1984) The origin of the eukaryotic cell. Specul Sci Technol 7:77–81

    CAS  Google Scholar 

  • Hartman H, Fedorov A (2002) The origin of the eukaryotic cell: a genomic investigation. Proc Natl Acad Sci U S A 90:1420–1425

    Article  CAS  Google Scholar 

  • Heimerl T, Flechsler J, Pickl C, Heinz V, Salecker B, Zweck J, Wanner G, Geimer S, Samson RY, Bell SD, Huber H, Wirth R, Wurch L, Podar M, Rachel R (2017) A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front Microbiol 8:1072

    Article  PubMed  PubMed Central  Google Scholar 

  • Hetzer MW (2010) The nuclear envelope. Cold Spring Harb Perspect Biol 2:a000539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holstein SE (2002) Clathrin and plant endocytosis. Traffic 3:614–620

    Article  CAS  PubMed  Google Scholar 

  • Horiike T, Hamada K, Kanaya S, Shinozawa T (2001) Origin of eukaryotic cell nuclei by symbiosis of Archaea in bacteria is revealed by homology-hit analysis. Nat Cell Biol 3:210–214

    Article  CAS  PubMed  Google Scholar 

  • Isermann P, Lammerding J (2017) Consequences of a tight squeeze: nuclear envelope rupture and repair. Nucleus 8:268–274

    Article  CAS  PubMed  Google Scholar 

  • Janota CS, Calero-Cuenca FJ, Costa J, Gomes ER (2017) SnapShot: nucleo-cytoskeletal interactions. Cell 169:970

    Article  CAS  PubMed  Google Scholar 

  • Jaspersen SL, Ghosh S (2012) Nuclear envelope insertion of spindle pole bodies and nuclear pore complexes. Nucleus 3:226–236

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karpov SA (2016) Flagellar apparatus structure of choanoflagellates. Cilia 5:11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Katta SS, Smoyer CJ, Jaspersen SL (2014) Destination: inner nuclear membrane. Trends Cell Biol 24:221–229

    Article  CAS  PubMed  Google Scholar 

  • Kee HL, Verhey KJ (2013) Molecular connections between nuclear and ciliary import processes. Cilia 2:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, Verhey KJ (2012) A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 14:431–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc B 365:729–748

    Article  CAS  Google Scholar 

  • Keeling PJ (2014) The impact of history on our perception of evolutionary events: endosymbiosis and the origin of eukaryotic complexity. Cold Spring Harb Perspect Biol 6:a016196

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kerney R, Kim E, Hangarter RP, Heiss AA, Bishop CD, Hall BK (2011) Intracellular invasion of green algae in a salamander host. Proc Natl Acad Sci U S A 108:6497–6502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim GH, Klotchkova TA, Kang Y-M (2001) Life without a cell membrane: regeneration of protoplasts from disintegrated cells of the marine green alga Bryopsis plumosa. J Cell Sci 114:2009–2014

    CAS  PubMed  Google Scholar 

  • Kim GH, Klotchkova TA, West JA (2002) From protoplasm to swarmer: regeneration of protoplasts from disintegrated cells of the multicellular marine green alga Microdictyon umbilicatum (Chlorophyta). J Phycol 38:174–183

    Article  Google Scholar 

  • Kind J, van Steensel B (2014) Stochastic genome-nuclear lamina interactions: modulating roles of lamin A and BAF. Nucleus 5:124–130

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitano H, Oda K (2006) Self-extending symbiosis: a mechanism for increasing robustness through evolution. Biol Theory 1:61–66

    Article  Google Scholar 

  • Klinger CM, Spang A, Dacks JB, Ettema TJ (2016) Tracing the Archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol 33:1528–1541

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Kanaizuka Y (1977) Reassembly of living cells from dissociated components in Bryopsis. Plant Cell Physiol 18:1373–1377

    Article  Google Scholar 

  • Koblenz B, Schoppmeier J, Grunow A, Lechtreck KF (2003) Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. J Cell Sci 116:2635–2646

    Article  CAS  PubMed  Google Scholar 

  • Kodama Y, Fujishima M (2010) Secondary symbiosis between Paramecium and Chlorella cells. Int Rev Cell Mol Biol 279:33–77

    Article  CAS  PubMed  Google Scholar 

  • Kollmar M (2015) Polyphyly of nuclear lamin genes indicates an early eukaryotic origin of the metazoan-type intermediate filament proteins. Sci Rep 5:10652

    Article  PubMed  PubMed Central  Google Scholar 

  • Koreny L, Field MC (2016) Ancient eukaryotic origin and evolutionary plasticity of nuclear lamina. Genome Biol Evol 8:2663–2671

    Article  PubMed  PubMed Central  Google Scholar 

  • Kronebusch PJ, Singer SJ (1987) The microtubule-organizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphase cardiac myocytes. J Cell Sci 88:25–34

    PubMed  Google Scholar 

  • Kutschera U, Niklas KJ (2005) Endosymbiosis, cell evolution, and speciation. Theory Biosci 124:1–24

    Article  CAS  PubMed  Google Scholar 

  • Lake JA (2011) Lynn Margulis (1938–2011). Nature 480:458

    Article  CAS  PubMed  Google Scholar 

  • Lake JA (2015) Eukaryotic origins. Philos Trans R Soc B 370:20140321

    Article  CAS  Google Scholar 

  • Lake JA, Rivera MC (1994) Was the nucleus the first endosymbiont? Proc Natl Acad Sci U S A 91:2880–2881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lake JA, Henderson E, Oakes M, Clark MW (1984) Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci U S A 81:3786–3790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane N (2017) Serial endosymbiosis or singular event at the origin of eukaryotes? J Theor Biol 434:58–67

    Article  PubMed  Google Scholar 

  • Lazcano A, Peretó J (2017) On the origin of mitosing cells: a historical appraisal of Lynn Margulis endosymbiotic theory. J Theor Biol 434:80–87

    Article  PubMed  Google Scholar 

  • Lee JY, Yoo BC, Lucas WJ (2000) Parallels between nuclear-pore and plasmodesmal tracking of information molecules. Planta 210:177–187

    Article  CAS  PubMed  Google Scholar 

  • Lindås AC, Valegård K, Ettema TJG (2017) Archaeal actin-family filament systems. Subcell Biochem 84:379–392

    Article  PubMed  Google Scholar 

  • Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Gao R, Li C, Ni J, Yang Z, Zhang Q, Chen H, Shen Y (2017) Functional assignment of multiple ESCRT-III homologs in cell division and budding in Sulfolobus islandicus. Mol Microbiol 105:540–553

    Article  CAS  PubMed  Google Scholar 

  • López-García P, Moreira D (2015) Open questions on the origin of eukaryotes. Trends Ecol Evol 30:697–708

    Article  PubMed  PubMed Central  Google Scholar 

  • Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Ding B, Van Der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125:435–476

    Article  Google Scholar 

  • Lyons S (2018) From cells to organisms: a history of cell theory. University of Toronto Press, Toronto

    Google Scholar 

  • Margulis L, Dolan MF, Guerrero R (2000) The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci U S A 97:6954–6959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin WF (2017) Physiology, anaerobes, and the origin of mitosing cells 50 years on. J Theor Biol 434:2–10

    Article  CAS  PubMed  Google Scholar 

  • Martin WF, Garg S, Zimorski V (2015) Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lond Ser B Biol Sci 370:20140330

    Article  CAS  Google Scholar 

  • Martin-Galiano AJ, Oliva MA, Sanz L, Bhattacharyya A, Serna M, Yebenes H, Valpuesta JM, Andreu J (2011) Bacterial tubulin distinct loop sequences and primitive assembly properties support its origin from a eukaryotic tubulin ancestor. J Biol Chem 286:19789–19803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattiroli F, Bhattacharyya S, Dyer PN, White AE, Sandman K, Burkhart BW, Byrne KR, Lee T, Ahn NG, Santangelo TJ, Reeve JN, Luger K (2017) Structure of histone-based chromatin in Archaea. Science 357:609–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazia D (1984) Centrosomes and mitotic poles. Exp Cell Res 153:1–15

    Article  CAS  PubMed  Google Scholar 

  • Mazia D (1987) The chromosome cycle and the centrosome cycle in the mitotic cycle. Int Rev Cytol 100:49–92

    Article  CAS  PubMed  Google Scholar 

  • Mazia D (1993) The cell cycle at the cellular level. Eur J Cell Biol 61(Suppl. 38):14

    Google Scholar 

  • McClure-Begley TD, Klymkowsky MW (2017) Nuclear roles for cilia-associated proteins. Cilia 6:8

    Article  PubMed  PubMed Central  Google Scholar 

  • McInally SG, Dawson SC (2016) Eight unique basal bodies in the multi-flagellated diplomonad Giardia lamblia. Cilia 5:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Midlej V, Benchimol M (2009) Giardia lamblia behavior during encystment: how morphological changes in shape occur. Parasitol Int 58:72–80

    Article  PubMed  Google Scholar 

  • Mizuno K (1993) Microtubule-nucleation sites on nuclei of higher plant cells. Protoplasma 173:77–85

    Article  Google Scholar 

  • Moog D, Maier UG (2017) Cellular compartmentation follows rules: the Schnepf theorem, its consequences and exceptions: a biological membrane separates a plasmatic from a non-plasmatic phase. Bioessays 39(8). doi:https://doi.org/10.1002/bies.201700030

  • Moore CE, Archibald JM (2009) Nucleomorph genomes. Annu Rev Genet 43:251–264

    Article  CAS  PubMed  Google Scholar 

  • Moreira D, López-García P (1998) Symbiosis between methanogenic archaea and delta-Proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol 47:517–530

    Article  CAS  PubMed  Google Scholar 

  • Nakayama T, Ishii T, Hotta T, Mizuno K (2008) Radial microtubule organization by histone H1 on nuclei of cultured tobacco BY-2 cells. J Biol Chem 283:16632–16640

    Article  CAS  PubMed  Google Scholar 

  • Nalabothula N, Xi L, Bhattacharyya S, Widom J, Wang JP, Reeve JN, Santangelo TJ, Fondufe-Mittendorf YN (2013) Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs. BMC Genomics 14:391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasir A, Kim KM, Caetano-Anollés G (2015) Lokiarchaeota: eukaryote-like missing links from microbial dark matter? Trends Microbiol 23:448–450

    Article  CAS  PubMed  Google Scholar 

  • Navarro AP, Collins MA, Folker ES (2016) The nucleus is a conserved mechanosensation and mechanoresponse organelle. Cytoskeleton 73:59–67

    Article  PubMed  Google Scholar 

  • Nicholson DJ (2010) Biological atomism and cell theory. Stud Hist Phil Biol Biomed Sci 41:202–211

    Article  Google Scholar 

  • Nickerson J (2001) Experimental observations of a nuclear matrix. J Cell Sci 114:463–474

    CAS  PubMed  Google Scholar 

  • O’Neil RM, La Claire JWII (1984) Mechanical wounding induces the formation of extensive coated membranes in giant cell. Science 255:331–333

    Article  Google Scholar 

  • Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522:236–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmos Y, Perdrix-Rosell A, Carlton JG (2016) Membrane binding by CHMP7 coordinates ESCRT-III-dependent nuclear envelope reformation. Curr Biol 26:2635–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267

    Article  CAS  PubMed  Google Scholar 

  • Onischenko E, Weis K (2011) Nuclear pore complex – a coat specifically tailored for the nuclear envelope. Curr Opin Cell Biol 23:293–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osorio DS, Gomes ER (2013) The contemporary nucleus: a trip down memory lane. Biol Cell 105:430–441

    Article  CAS  PubMed  Google Scholar 

  • Pak JY, Solorzano C, Arai M, Nitta T (1991) Two distinct steps for spontaneous generation of subprotoplasts from a disintegrated Bryopsis cell. Plant Physiol 96:819–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pederson T (2000) Half a century of the nuclear matrix. Mol Biol Cell 11:799–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira SL, Reeve JN (1998) Histones and nucleosomes in Archaea and Eukarya: a comparative analysis. Extremophiles 2:141–148

    Article  CAS  PubMed  Google Scholar 

  • Peter A, Stick R (2015) Evolutionary aspects in intermediate filament proteins. Curr Opin Cell Biol 32:48–55

    Article  CAS  PubMed  Google Scholar 

  • Petrovská B, Šebela M, Doležel J (2015) Inside a plant nucleus: discovering the proteins. J Exp Bot 66:1627–1640

    Article  PubMed  CAS  Google Scholar 

  • Pilhofer M, Ladinsky MS, McDowall AW, Petroni G, Jensen GJ (2011) Microtubules in bacteria: ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol 9:e1001213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polo S, Di Fiore PP (2006) Endocytosis conducts the cell signaling orchestra. Cell 124:897–900

    Article  CAS  PubMed  Google Scholar 

  • Potter C, Zhu W, Razafsky D, Ruzycki P, Kolesnikov AV, Doggett T, Kefalov VJ, Betleja E, Mahjoub MR, Hodzic D (2017) Multiple isoforms of nesprin1 are integral components of ciliary rootlets. Curr Biol 27:2014–2022

    Article  CAS  PubMed  Google Scholar 

  • Qiu H, Yoon HS, Bhattacharya D (2013) Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes. Front Plant Sci 4:366

    Article  PubMed  PubMed Central  Google Scholar 

  • Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Duménil AM, Manel N, Piel M (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352:359–362

    Article  CAS  PubMed  Google Scholar 

  • Reeve JN, Bailey KA, Li WT, Marc F, Sandman K, Soares DJ (2004) Archaeal histones: structures, stability and DNA binding. Biochem Soc Trans 32:227–230

    Article  CAS  PubMed  Google Scholar 

  • Resendes KK, Rasala BA, Forbes DJ (2008) Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export. Mol Cell Biol 28:1755–1769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieder CL, Faruki S, Khodjakov A (2001) The centrosome in vertebrates: more than a microtubule-organizing center. Trends Cell Biol 11:413–419

    Article  CAS  PubMed  Google Scholar 

  • Rikhy R, Mavrakis M, Lippincott-Schwartz J (2015) Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo. Biol Open 4:301–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MS (2015) Forty years of clathrin-coated vesicles. Traffic 16:1210–1238

    Article  CAS  PubMed  Google Scholar 

  • Rochette NC, Brochier-Armanet C, Gouy M (2014) Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol Biol Evol 31:832–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rout MP, Field MC (2017) The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu Rev Biochem 86:637–657

    Article  CAS  PubMed  Google Scholar 

  • Rout S, Zumthor JP, Schraner EM, Faso C, Heh AB (2016) An interactome-centered protein discovery approach reveals novel components involved in mitosome function and homeostasis in Giardia lamblia. PLoS Pathog 12:e1006036

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ruegg MA (2005) Organization of synaptic myonuclei by Syne proteins and their role during the formation of the nerve-muscle synapse. Proc Natl Acad Sci U S A 102:5643–5644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rüthnick D, Neuner A, Dietrich F, Kirrmaier D, Engel U, Knop M, Schiebel E (2017) Characterization of spindle pole body duplication reveals a regulatory role for nuclear pore complexes. J Cell Biol 216:2425–2442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sachs J (1892a) Beiträge zur Zellentheorie. Energiden und Zellen. Flora 75:57–67

    Google Scholar 

  • Sachs J (1892b) Weitere Betrachtungen über Energiden und Zellen. Flora 81:405–434

    Google Scholar 

  • Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:225–274

    Article  CAS  Google Scholar 

  • Salisbury JL (1988) The lost neuromotor apparatus of Chlamydomonas: rediscovered. J Protozool 35:574–577

    Article  CAS  PubMed  Google Scholar 

  • Salisbury JL, Baron AT, Sanders MA (1988) The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. J Cell Biol 107:635–641

    Article  CAS  PubMed  Google Scholar 

  • Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433

    Article  PubMed  CAS  Google Scholar 

  • Samson RY, Bell SD (2016) Archaeal DNA replication origins and recruitment of the MCM replicative helicase. Enzymes 39:169–190

    Article  CAS  PubMed  Google Scholar 

  • Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in archaea. Science 322:1710–1713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samson RY, Abeyrathne PD, Bell SD (2016) Mechanism of archaeal MCM helicase recruitment to DNA replication origins. Mol Cell 61:287–296

    Article  CAS  PubMed  Google Scholar 

  • Samson RY, Dobro MJ, Jensen GJ, Bell SD (2017) The structure, function and roles of the archaeal ESCRT apparatus. Subcell Biochem 84:357–377

    Article  PubMed  Google Scholar 

  • Sapp J, Carrapiço F, Zolotonosov M (2002) Symbiogenesis: the hidden face of Constantin Merezhkowsky. Hist Philos Life Sci 24:413–440

    Article  PubMed  Google Scholar 

  • Scheer U (2017) Historical roots of centrosome research: discovery of Boveri’s microscope slides in Würzburg. Philos Trans R Soc B 369:20130469

    Article  Google Scholar 

  • Schiel JA, Childs C, Prekeris R (2013) Endocytic transport and cytokinesis: from regulation of the cytoskeleton to midbody inheritance. Trends Cell Biol 23:319–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlieper D, Oliva MA, Andreu JM, Löwe J (2005) Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci U S A 1024:9170–9175

    Article  CAS  Google Scholar 

  • Schmit AC (2002) Acentrosomal microtubule nucleation in higher plants. Int Rev Cytol 220:257–289

    Article  CAS  PubMed  Google Scholar 

  • Scita G, Di Fiore PP (2010) The endocytic matrix. Nature 463:464–473

    Article  CAS  PubMed  Google Scholar 

  • Sezgin E, Levental I, Mayor S, Eggeling C (2017) The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Biol 18:361–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherlekar A, Rikhy R (2016) Syndapin promotes pseudocleavage furrow formation by actin organization in the syncytial Drosophila embryo. Mol Biol Cell 27:2064–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Shiflett AM, Johnson PJ (2010) Mitochondrion-related organelles in eukaryotic protists. Annu Rev Microbiol 64:409–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimamura M, Brown RC, Lemmon BE, Akashi T, Mizuno K, Nishihara N, Tomizawa K, Yoshimoto K, Deguchi H, Hosoya H, Horio T, Mineyuki Y (2004) Gamma-tubulin in basal land plants: characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16:45–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigismund S, Confalonieri S, Ciliberto A, Polo S, Scita G, Di Fiore PP (2012) Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol Rev 92:273–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon DN, Wilson KL (2011) The nucleoskeleton as a genome-associated dynamic ‘network of networks’. Nat Rev Mol Cell Biol 12:695–708

    Article  CAS  PubMed  Google Scholar 

  • Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3:a004697

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simons K, Vaz WL (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33:269–295

    Article  CAS  PubMed  Google Scholar 

  • Smetana K, Steele WJ, Busch H (1963) A nuclear ribonucleoprotein network. Exp Cell Res 31:198–201

    Article  Google Scholar 

  • Smoyer CJ, Katta SS, Gardner JM, Stoltz L, McCroskey S, Bradford WD, McClain M, Smith SE, Slaughter BD, Unruh JR, Jaspersen SL (2016) Analysis of membrane proteins localizing to the inner nuclear envelope in living cells. J Cell Biol 215:575–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokac AM, Wieschaus E (2008a) Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell 14:775–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokac AM, Wieschaus E (2008b) Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J Cell Sci 121:1815–1824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song C, Murata K, Suzaki T (2017) Intracellular symbiosis of algae with possible involvement of mitochondrial dynamics. Sci Rep 7:1221

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spang A, Martijn J, Saw JH, Lind AE, Guy L, Ettema TJ (2013) Close encounters of the third domain: the emerging genomic view of archaeal diversity and evolution. Archaea 2013:202358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spang A, Caceres EF, Ettema TJG (2017) Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357. https://doi.org/10.1126/science.aaf3883

  • Srsen V, Fant X, Heald R, Rabouille C, Merdes A (2009) Centrosome proteins form an insoluble perinuclear matrix during muscle cell differentiation. BMC Cell Biol 10:28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stoppin V, Vantard M, Schmit AC, Lambert AM (1994) Isolated plant nuclei nucleate microtubule assembly: the nuclear surface in higher plants has centrosome-like activity. Plant Cell 6:1099–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surkont J, Pereira-Leal JB (2016) Are there Rab GTPases in Archaea? Mol Biol Evol 33:1833–1842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taillon BE, Adler SA, Suhan JP, Jarvik JW (1992) Mutational analysis of centrin: an EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas. J Cell Biol 119:1613–1624

    Article  CAS  PubMed  Google Scholar 

  • Takao D, Verhey KJ (2016) Gated entry into the ciliary compartment. Cell Mol Life Sci 73:119–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takao D, Dishinger JF, Kee HL, Pinskey JM, Allen BL, Verhey KJ (2014) An assay for clogging the ciliary pore complex distinguishes mechanisms of cytosolic and membrane protein entry. Curr Biol 24:2288–2294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takao D, Wang L, Boss A, Verhey KJ (2017) Protein interaction analysis provides a map of the spatial and temporal organization of the cliary gating zone. Curr Biol 27:2296–2306

    Article  CAS  PubMed  Google Scholar 

  • Tan SY, Brown J (2006) Rudolph Virchow (1821–1902): Pope of pathology. Singap Med J 47:567–568

    CAS  Google Scholar 

  • Tapley EC, Starr DA (2013) Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr Opin Cell Biol 25:57–62

    Article  CAS  PubMed  Google Scholar 

  • Tassin AM, Maro B, Bornens M (1985) Fate of microtubule-organizing centers during myogenesis in vitro. J Cell Biol 100:35–46

    Article  CAS  PubMed  Google Scholar 

  • Taylor FJR (1974) Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23:229–258

    Article  Google Scholar 

  • Taylor FJR (1976) Autogenous theories for the origin of eukaryotes. Taxon 25:377–468

    Article  Google Scholar 

  • Torrado B, Graña M, Badano JL, Irigoín F (2016) Ciliary entry of the Hedgehog transcriptional activator Gli2 is mediated by the nuclear import machinery but differs from nuclear transport in being Imp-α/β1-independent. PLoS One 11:e0162033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Touz MC, Zamponi N (2017) Sorting without a Golgi complex. Traffic 18:604–621

    Article  PubMed  CAS  Google Scholar 

  • Trépout S, Wehenkel AM (2017) Bacterial tubulins: a eukaryotic-like microtubule cytoskeleton. Trends Microbiol 25:782–784. https://doi.org/10.1016/j.tim.2017.08.004

    Article  PubMed  CAS  Google Scholar 

  • Ungricht R, Kutay U (2015) Establishment of NE asymmetry – targeting of membrane proteins to the inner nuclear membrane. Curr Opin Cell Biol 34:135–141

    Article  CAS  PubMed  Google Scholar 

  • Ungricht R, Kutay U (2017) Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol 18:229–245

    Article  CAS  PubMed  Google Scholar 

  • van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56:221–231

    Article  PubMed  CAS  Google Scholar 

  • van Steensel B, Belmont AS (2017) Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169:780–791

    Article  PubMed  CAS  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Verma DPS, Miao GH, Joshi CP, Cheon C, Delauney A (1991) Internalization of Rhizobium by plant cells: targeting and role of peribacteroid membrane nodulins. In: Herrmann RG, Larkins B (eds) NATO ASI book series, Plant molecular biology, vol 2. Plenum Press, New York, pp 121–130

    Google Scholar 

  • Vertii A, Hehnly H, Doxsey S (2016) The centrosome, a multitalented renaissance organelle. Cold Spring Harb Perspect Biol 8:a025049

    Article  PubMed  Google Scholar 

  • Vietri M, Stenmark H, Campsteijn C (2016) Closing a gap in the nuclear envelope. Curr Opin Cell Biol 40:90–97

    Article  CAS  PubMed  Google Scholar 

  • Voleman L, Najdrová V, Ástvaldsson Á, Tůmová P, Einarsson E, Švindrych Z, Hagen GM, Tachezy J, Svärd SG, Doležal P (2017) Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum. BMC Biol 15:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen J, Li J (1998) Nuclear matrix of the most primitive eukaryote Archezoa. Sci China C Life Sci 43:479–486

    Article  Google Scholar 

  • Williams TA, Embley TM (2014) Archaeal “dark matter” and the origin of eukaryotes. Genome Biol Evol 6:474–481

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236

    Article  CAS  PubMed  Google Scholar 

  • Wilson EB (1925) The cell in development and heredity. Macmillan, New York

    Google Scholar 

  • Wilson KL, Dawson SC (2011) Evolution: functional evolution of nuclear structure. J Cell Biol 195:171–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci U S A 99:8742–8747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR (2004a) A new biology for a new century. Microbiol Mol Biol Rev 68:173–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR (2004b) The archaeal concept and the world it lives in: a retrospective. Photosynth Res 80:361–372

    Article  CAS  PubMed  Google Scholar 

  • Wright RL, Adler SA, Spanier JG, Jarvik JW (1989) Nucleus-basal body connector in Chlamydomonas: evidence for a role in basal body segregation and against essential roles in mitosis or in determining cell polarity. Cell Motil Cytoskeleton 14:516–526

    Article  CAS  PubMed  Google Scholar 

  • Yamada M, Goshima G (2017) Mitotic spindle assembly in land plants: molecules and mechanisms. Biology (Basel) 6:E6

    Google Scholar 

  • Yubuki N, Leander BS (2013) Evolution of microtubule organizing centers across the tree of eukaryotes. Plant J 75:230–244

    Article  CAS  PubMed  Google Scholar 

  • Zamponi N, Zamponi E, Mayol GF, Lanfredi-Rangel A, Svärd SG, Touz MC (2017) Endoplasmic reticulum is the sorting core facility in the Golgi-lacking protozoan Giardia lamblia. Traffic 18:604–621

    Article  CAS  PubMed  Google Scholar 

  • Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L, Vancaester E, Seitz KW, Anantharaman K, Starnawski P, Kjeldsen KU, Stott MB, Nunoura T, Banfield JF, Schramm A, Baker BJ, Spang A, Ettema TJ (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M (2007) Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134:901–908

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Burki F, Bråte J, Keeling PJ, Klaveness D, Shalchian-Tabrizi K (2012) Collodictyon – an ancient lineage in the tree of eukaryotes. Mol Biol Evol 29:1557–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zubáčová Z, Novák L, Bublíková J, Vacek V, Fousek J, Rídl J, Tachezy J, Doležal P, Vlček C, Hampl V (2013) The mitochondrion-like organelle of Trimastix pyriformis contains the complete glycine cleavage system. PLoS One 8:e55417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zumthor JP, Cernikova L, Rout S, Kaech A, Faso C, Hehl AB (2016) Static clathrin assemblies at the peripheral vacuole-plasma membrane interface of the parasitic protozoan Giardia lamblia. PLoS Pathog 12:e1005756

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Baluška, F., Lyons, S. (2018). Symbiotic Origin of Eukaryotic Nucleus: From Cell Body to Neo-Energide. In: Sahi, V., Baluška, F. (eds) Concepts in Cell Biology - History and Evolution. Plant Cell Monographs, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-319-69944-8_3

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